Deciphering the impact of endoparasitic infection on immune response and gut microbial composition of Channa punctata

Intestinal parasitic infections caused by helminths are globally distributed and are a major cause of morbidity worldwide. Parasites may modulate the virulence, gut microbiota diversity and host responses during infection. Despite numerous works, little is known about the complex interaction between...

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Main Authors: Vikash Kumar, Suvra Roy, Satya Narayan Parida, Kampan Bisai, Souvik Dhar, Asim Kumar Jana, Basanta Kumar Das
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-02-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2024.1296769/full
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author Vikash Kumar
Suvra Roy
Satya Narayan Parida
Kampan Bisai
Souvik Dhar
Asim Kumar Jana
Basanta Kumar Das
author_facet Vikash Kumar
Suvra Roy
Satya Narayan Parida
Kampan Bisai
Souvik Dhar
Asim Kumar Jana
Basanta Kumar Das
author_sort Vikash Kumar
collection DOAJ
description Intestinal parasitic infections caused by helminths are globally distributed and are a major cause of morbidity worldwide. Parasites may modulate the virulence, gut microbiota diversity and host responses during infection. Despite numerous works, little is known about the complex interaction between parasites and the gut microbiota. In the present study, the complex interplay between parasites and the gut microbiota was investigated. A total of 12 bacterial strains across four major families, including Enterobacteriaceae, Morganellaceae, Flavobacteriaceae, and Pseudomonadaceae, were isolated from Channa punctata, infected with the nematode species Aporcella sp., Axonchium sp., Tylencholaimus mirabilis, and Dioctophyme renale. The findings revealed that nematode infection shaped the fish gut bacterial microbiota and significantly affected their virulence levels. Nematode-infected fish bacterial isolates are more likely to be pathogenic, with elevated hemolytic activity and biofilm formation, causing high fish mortality. In contrast, isolates recovered further from non-parasitised C. punctata were observed to be non-pathogenic and had negligible hemolytic activity and biofilm formation. Antibiogram analysis of the bacterial isolates revealed a disproportionately high percentage of bacteria that were either marginally or multidrug resistant, suggesting that parasitic infection-induced stress modulates the gut microenvironment and enables colonization by antibiotic-resistant strains. This isolation-based study provides an avenue to unravel the influence of parasitic infection on gut bacterial characteristics, which is valuable for understanding the infection mechanism and designing further studies aimed at optimizing treatment strategies. In addition, the cultured isolates can supplement future gut microbiome studies by providing wet lab specimens to compare (meta)genomic information discovered within the gut microenvironment of fish.
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spelling doaj.art-ed4dfdf77f174cb2b6f8edf34b086eee2024-02-27T04:39:04ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882024-02-011410.3389/fcimb.2024.12967691296769Deciphering the impact of endoparasitic infection on immune response and gut microbial composition of Channa punctataVikash KumarSuvra RoySatya Narayan ParidaKampan BisaiSouvik DharAsim Kumar JanaBasanta Kumar DasIntestinal parasitic infections caused by helminths are globally distributed and are a major cause of morbidity worldwide. Parasites may modulate the virulence, gut microbiota diversity and host responses during infection. Despite numerous works, little is known about the complex interaction between parasites and the gut microbiota. In the present study, the complex interplay between parasites and the gut microbiota was investigated. A total of 12 bacterial strains across four major families, including Enterobacteriaceae, Morganellaceae, Flavobacteriaceae, and Pseudomonadaceae, were isolated from Channa punctata, infected with the nematode species Aporcella sp., Axonchium sp., Tylencholaimus mirabilis, and Dioctophyme renale. The findings revealed that nematode infection shaped the fish gut bacterial microbiota and significantly affected their virulence levels. Nematode-infected fish bacterial isolates are more likely to be pathogenic, with elevated hemolytic activity and biofilm formation, causing high fish mortality. In contrast, isolates recovered further from non-parasitised C. punctata were observed to be non-pathogenic and had negligible hemolytic activity and biofilm formation. Antibiogram analysis of the bacterial isolates revealed a disproportionately high percentage of bacteria that were either marginally or multidrug resistant, suggesting that parasitic infection-induced stress modulates the gut microenvironment and enables colonization by antibiotic-resistant strains. This isolation-based study provides an avenue to unravel the influence of parasitic infection on gut bacterial characteristics, which is valuable for understanding the infection mechanism and designing further studies aimed at optimizing treatment strategies. In addition, the cultured isolates can supplement future gut microbiome studies by providing wet lab specimens to compare (meta)genomic information discovered within the gut microenvironment of fish.https://www.frontiersin.org/articles/10.3389/fcimb.2024.1296769/fullendoparasitic infectionfishgut microbiotabacterial phenotypeimmune response
spellingShingle Vikash Kumar
Suvra Roy
Satya Narayan Parida
Kampan Bisai
Souvik Dhar
Asim Kumar Jana
Basanta Kumar Das
Deciphering the impact of endoparasitic infection on immune response and gut microbial composition of Channa punctata
Frontiers in Cellular and Infection Microbiology
endoparasitic infection
fish
gut microbiota
bacterial phenotype
immune response
title Deciphering the impact of endoparasitic infection on immune response and gut microbial composition of Channa punctata
title_full Deciphering the impact of endoparasitic infection on immune response and gut microbial composition of Channa punctata
title_fullStr Deciphering the impact of endoparasitic infection on immune response and gut microbial composition of Channa punctata
title_full_unstemmed Deciphering the impact of endoparasitic infection on immune response and gut microbial composition of Channa punctata
title_short Deciphering the impact of endoparasitic infection on immune response and gut microbial composition of Channa punctata
title_sort deciphering the impact of endoparasitic infection on immune response and gut microbial composition of channa punctata
topic endoparasitic infection
fish
gut microbiota
bacterial phenotype
immune response
url https://www.frontiersin.org/articles/10.3389/fcimb.2024.1296769/full
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